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Research ArticleResearch Article: New Research, Cognition and Behavior

Coding Dynamics of the Striatal Networks During Learning

Maxime Villet, Patricia Reynaud-Bouret, Julien Poitreau, Jacopo Baldi, Sophie Jaffard, Ashwin James, Alexandre Muzy, Evgenia Kartsaki, Gilles Scarella, Francesca Sargolini and Ingrid Bethus
eNeuro 30 September 2024, 11 (10) ENEURO.0436-23.2024; https://doi.org/10.1523/ENEURO.0436-23.2024
Maxime Villet
1Université Côte d’Azur, CNRS, INSERM, Institut de Pharmacologie Moléculaire et Cellulaire, Valbonne 06560, France
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Patricia Reynaud-Bouret
2Université Côte d’Azur, CNRS, LJAD and NeuroMod, Nice 0600, France
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Julien Poitreau
3CRPN, UMR 7077, Aix-Marseille University, CNRS, Marseille 13331, France
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Jacopo Baldi
1Université Côte d’Azur, CNRS, INSERM, Institut de Pharmacologie Moléculaire et Cellulaire, Valbonne 06560, France
2Université Côte d’Azur, CNRS, LJAD and NeuroMod, Nice 0600, France
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Sophie Jaffard
2Université Côte d’Azur, CNRS, LJAD and NeuroMod, Nice 0600, France
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Ashwin James
4Université Côte d’Azur, CNRS, I3S, Valbonne 06560, France
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Alexandre Muzy
4Université Côte d’Azur, CNRS, I3S, Valbonne 06560, France
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Evgenia Kartsaki
5Université Côte d’Azur, NeuroMod, Valbonne 06560, France
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Gilles Scarella
2Université Côte d’Azur, CNRS, LJAD and NeuroMod, Nice 0600, France
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Francesca Sargolini
3CRPN, UMR 7077, Aix-Marseille University, CNRS, Marseille 13331, France
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Ingrid Bethus
1Université Côte d’Azur, CNRS, INSERM, Institut de Pharmacologie Moléculaire et Cellulaire, Valbonne 06560, France
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Abstract

The rat dorsomedial (DMS) and dorsolateral striatum (DLS), equivalent to caudate nucleus and putamen in primates, are required for goal-directed and habit behaviour, respectively. However, it is still unclear whether and how this functional dichotomy emerges in the course of learning. In this study, we investigated this issue by recording DMS and DLS single neuron activity in rats performing a continuous spatial alternation task, from the acquisition to optimized performance. We first applied a classical analytical approach to identify task-related activity based on the modifications of single neuron firing rate in relation to specific task events or maze trajectories. We then used an innovative approach based on Hawkes process to reconstruct a directed connectivity graph of simultaneously recorded neurons, that was used to decode animal behavior. This approach enabled us to better unravel the role of DMS and DLS neural networks across learning stages. We showed that DMS and DLS display different task-related activity throughout learning stages, and the proportion of coding neurons over time decreases in the DMS and increases in the DLS. Despite these major differences, the decoding power of both networks increases during learning. These results suggest that DMS and DLS neural networks gradually reorganize in different ways in order to progressively increase their control over the behavioral performance.

Footnotes

  • The authors declare no competing financial interests.

  • This work was supported by the French government, through the UCAJedi and 3IA Côte d’Azur Investissements d’Avenir managed by the National Research Agency (ANR-15- IDEX-01 and ANR-19-P3IA-0002), by the interdisciplinary Institute for Modeling in Neuroscience and Cognition (NeuroMod) of the Université Côte d’Azur and directly by the National Research Agency ANR-08-JCJC-0125-01, ANR-19-CE40-0024 with the ChaMaNe project, MITI AAP “défi modélisation du vivant” with DYNAMO project and AAP 80PRIME with eXpLAIn. It is part of the Computabrain project.

  • ↵*These authors contributed equally to this work.

  • ↵#These authors contributed equally to this work.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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Coding Dynamics of the Striatal Networks During Learning
Maxime Villet, Patricia Reynaud-Bouret, Julien Poitreau, Jacopo Baldi, Sophie Jaffard, Ashwin James, Alexandre Muzy, Evgenia Kartsaki, Gilles Scarella, Francesca Sargolini, Ingrid Bethus
eNeuro 30 September 2024, 11 (10) ENEURO.0436-23.2024; DOI: 10.1523/ENEURO.0436-23.2024

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Coding Dynamics of the Striatal Networks During Learning
Maxime Villet, Patricia Reynaud-Bouret, Julien Poitreau, Jacopo Baldi, Sophie Jaffard, Ashwin James, Alexandre Muzy, Evgenia Kartsaki, Gilles Scarella, Francesca Sargolini, Ingrid Bethus
eNeuro 30 September 2024, 11 (10) ENEURO.0436-23.2024; DOI: 10.1523/ENEURO.0436-23.2024
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